Brachyteles hypoxanthus

Brief Report Folia Primatol 2005;76:33–36 DOI: 10.1159/000082453

Age-Related Variation in Copulations of Male Northern Muriquis (Brachyteles hypoxanthus) Carla B. Possamaia, b Robert J. Youngb Sergio L. Mendes d Karen B. Striere

Regiane C.R. de Oliveiraa, c

a Estação Biológica de Caratinga/RPPN-FMA, Ipanema, Minas Gerais, b Conservation, Ecology and Animal Behaviour Group, PUC-Minas, Belo Horizonte, Minas Gerais, c Instituto de Pesquisas Ecológicas (IPE), Nazaré Paulista and d Departamento de Biologia, Universidade Federal de Espírito Santo, Vitoria, Brazil; e Department of Anthropology, University of Wisconsin, Madison, Wisc., USA

Key Words Brachyteles hypoxanthus ` Sexual behavior, age-related

Introduction

Northern muriquis (Brachyteles hypoxanthus) live in a multi-male and multifemale society where sexual behavior is characterized by promiscuity and lack of aggression between males for access to females [Strier, 1992]. Copulations may occur throughout the year, but both sexual behavior and conceptions show pronounced seasonality [Strier, 1997; Strier et al., 2003]. Previous studies indicated that copulation frequencies did not differ between males of different age classes, but that copulations of older males were more likely to terminate with ejaculation than those of younger males, and copulations with ejaculate lasted longer than those without ejaculate [Strier, 1997; Strier et al., 2002]. Goodall [1986] suggested that pseudo-copulation in chimpanzees, Pan troglodytes, may have a function in social bonding and play. Ren et al. [1995] found that although captive golden monkeys, Rhinopithecus roxellana roxellana, copulate year-round, ejaculations are confined to the reproductive season. Copulations without ejaculate in muriquis could therefore serve a social function instead of, or in addition to, reflecting physiological processes associated with reproductive maturation. Here, we use new data to examine whether age-related differences in muriqui copulation patterns occur year-round or are restricted to months in which conceptions occur.

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Karen B. Strier, Department of Anthropology 1180 Observatory Drive, University of Wisconsin Madison, WI 53706 (USA) Tel. +1 608 262 0302, Fax +1 608 265 4216 E-Mail [email protected]

Methods Copulation data were collected over a 17-month period from October 2001 through February 2003 as part of an ongoing muriqui study at the Estação Biológica de Caratinga/ RPPN Feliciano Miguel Abdala, Minas Gerais, Brazil. Our subjects were members of the Matão group, which has been monitored systematically since June 1982. During the present study, there were up to 74 members in the group, with 21 adult females, 4 nulliparous females that had recently immigrated, 19 adult males, and 30 immatures of various sex-age classes. All group members are well habituated and can be identified individually by the natural markings of their faces and fur. Ages are known for all but one male, who was already present as an adult in 1982 and is estimated to have been ≥30 years old during this study. Whenever visibility permitted, we recorded the identities of both participants, the duration of the copulation to the nearest second, and whether or not the copulation terminated with ejaculate. Copulations are defined by mounting-intromission-thrusting sequences, and are easily distinguishable from all other activities. Ejaculation, when it occurs, results in the production of a large, highly visible copulatory plug in this genus [Milton, 1985; Strier, 1986, 1997]. We distinguished conception months (CMs, n = 7) from nonconception months (NCMs, n = 10) by subtracting gestation length (7.2 months, per Strier and Ziegler, 1997] from the dates on which subsequent births occurred.

Results

A total of 354 copulations was observed from October 2001 through February 2003, with a median of 17 copulations per male (mean = 18.6 ± 7.2, min–max = 2– 29, n = 19; table 1). Copulation frequencies were not significantly correlated with male age (rs = 0.18, n = 19, p > 0.05). Of the 309 copulations for which the presence or absence of ejaculate could be determined, 215 (69.6%) terminated with ejaculate and 94 (30.4%) terminated without ejaculate (table 1). The frequency of copulations with ejaculate increased with male age (rs = 0.67, n = 18, p < 0.01), while that of copulations without ejaculate decreased with male age (rs = –0.54, n = 18, p < 0.05). Copulation durations were determined for 207 (96.3%) of the copulations with ejaculate, and for all 94 copulations without ejaculate. Median copulation durations were significantly longer for copulations with ejaculate (3.92 min) than without (2.42 min; Wilcoxon z = 2.44, n = 17, p = 0.015), but there was no relationship between male age and the median duration of copulations with ejaculate (rs = –0.47, n = 18, p > 0.05) or without ejaculate (rs = –0.265, n = 18, p > 0.05). Of copulations for which the presence or absence of ejaculation was scored, 221 (71.5%) occurred during CMs and 88 (28.5%) occurred during NCMs. A significantly higher proportion of the copulations during CMs terminated with ejaculate (median = 0.86, n = 18) than copulations during NCMs (median = 0.69, n = 18; Wilcoxon z = –2.04, n = 18, p < 0.05). The proportion of copulations with ejaculate increased significantly with male age during CMs (rs = 0.72, n = 18, p < 0.01), but not during NCMs (rs = 0.39, n = 18, p > 0.05). Similarly, the median duration of copulations with ejaculate decreased significantly with male age during CMs (rs = –0.49, n = 18, p < 0.05) but not during the NCMs (rs = –0.33, n = 15, p > 0.05).

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Folia Primatol 2005;76:33–36

Possamai/Young/de Oliveira/Mendes/Strier

Table 1. Distribution of copulations by male age Male ID

=Age =years

Total n

NR PE HO IN NO TL AG CO JR TH BE BLK RB NE DA AM DI NI IV

= 7 = 7 = 8 = 9 =10 =11 =12 =12 =12 =13 =14 =14 =15 =16 =17 =18 =21 =21 ³30

2 15 10 27 21 29 17 16 17 20 28 16 15 24 26 8 26 22 15

0 1 0 1 6 5 5 1 2 0 5 1 1 5 4 0 3 5 0

0 4 2 8 13 13 9 13 10 6 18 15 13 17 19 7 21 14 13

354

45

215

Total

Ejaculate unknown n

With ejaculate

Without ejaculate

n

median duration min

n

median duration min

* 10.98 8.75 4.88 2.13 4.23 1.90 3.52 4.24 4.07 2.98 5.42 4.02 4.23 2.63 2.25 3.83 3.73 3.24

2 10 8 18 2 11 3 2 5 14 5 0 1 2 3 1 2 3 2

4.86 7.08 2.13 2.30 4.46 1.17 2.57 2.05 4.53 1.55 2.55 * 1.33 1.52 3.47 0.42 1.33 3.08 4.58

94

* No copulations of this type.

Discussion

Consistent with previous findings, we found no relationship between male age and copulation frequencies in this study. Ejaculation frequencies and the proportion of copulations that terminated with ejaculate were positively related to male age, but these relationships appear to be restricted to CMs; during the CMs older males also achieved their ejaculations significantly faster than younger males. Together, these data emphasize the importance of distinguishing copulations by whether or not they terminate with ejaculation, and raise new questions about the potential contributions of male age and experience, as well as female cooperation, on variation in the sexual and reproductive behavior of male muriquis. The ability to achieve ejaculations rapidly might explain why the copulations of older males were more likely to terminate with ejaculate than those of younger males. However, if the shorter copulation-to-ejaculation latencies of older, more experienced males are solely a reflection of faster physiological responses, we would have expected to find evidence for similar age-related effects during both NCMs and CMs. Instead, we found that age-related effects on copulation durations were restricted to CMs, suggesting that either older males are more proficient at detecting female reproductive condition and responding to subtle shifts in female behavior associated with fertility, or that female muriquis, like many other female Copulation of Muriquis Varies with Age


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primates [e.g., Smuts, 1985; Manson, 1997] alter their behavior depending on their preferences for particular partners. Acknowledgments We are grateful to the Brazilian government and CNPq for permission to conduct research in Brazil. We also thank E.M. Veado for providing logistical support, and J. Gomes for his help in all aspects of the fieldwork. This study was funded by grants to K.B.S. from the Liz Claiborne and Art Ortenberg Foundation, the Margot Marsh Biodiversity Foundation, the National Geographic Society, and the Graduate School of the University of Wisconsin-Madison. E. Veado, J. Gomes, F. Mendes, J. Rímoli, A.O. Rímoli, F. Neri, P. Coutinho, A. Carvalho, L. Oliveira, C. Nogueira, S. Neto, W. Teixeira, R. Printes, M. Maciel, C. Costa, A. Oliva, L. Dib, D. Carvalho, N. Bejar, C. Coelho, L. Dias, V.O. Guimaraes, W. Martins, J.C. da Silva, F.P. Paim, and M.F. Iurck contributed to the long-term demographic data. References Goodall J (1986). The Chimpanzees of Gombe: Patterns of Behavior. Cambridge, MA, Harvard University Press. Manson JH (1997). Primate consortships: A critical review. Current Anthropology 38: 353–374. Milton K (1985). Mating patterns of woolly spider monkeys, Brachyteles arachnoides: Implications for female choice. Behavioral Ecology and Sociobiology 17: 53–59. Ren RM, Yan KH, Su YJ, Qi HJ, Liang B, Bao WY, de Waal FBM (1995). The reproductive behaviour of golden monkeys in captivity (Rhinopithecus roxellana roxellana). Primates 36: 135–143. Smuts BB (1985). Sex and Friendship in Baboons. New York, Aldine. Strier KB (1986). Reprodução de Brachyteles arachnoides (Primates, Cebidae). In A Primatologia no Brasil (Thiago de Mello M, ed.), vol 2, pp 163–175. Brasilia, Sociedade Brasileira de Primatologia. Strier KB (1992). Causes and consequences of nonaggression in woolly spider monkeys. In Aggression and Peacefulness in Humans and Other Primates (Silverberg J, Gray JP, eds.), pp 100–116. New York, Oxford University Press. Strier KB (1997). Mate preference of wild muriqui monkeys (Brachyteles arachnoides): Reproductive and social correlates. Folia Primatologica 68: 120–133. Strier KB, Ziegler TE (1997). Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys, Brachyteles arachnoides. American Journal of Primatology 42: 299–310. Strier KB, Dib LT, Figueira JE (2002). Social dynamics of male muriquis (Brachyteles arachnoides hypoxanthus). Behaviour 139: 315–342. Strier KB, Lynch JW, Ziegler TE (2003). Hormonal changes during the mating and conception seasons of wild northern muriquis (Brachyteles arachnoides hypoxanthus). American Journal of Primatology 61: 85–99.

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Possamai/Young/de Oliveira/Mendes/Strier